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Cah. Biol. Mar. (2019) 60 : 189-194 DOI: 10.21411/CBM.A.23607FF9

First documented smoothback Squatina oculata Bonaparte, 1840 from the North-Eastern Mediterranean Sea, Turkey

Deniz ERGÜDEN 1, Deniz AYAS 2, Mevlut GÜRLEK 1, Serpil KARAN 1 and Cemal TURAN 1 (1) Molecular Ecology and Fisheries Genetic Laboratory, Faculty of Marine Sciences and Technology, Iskenderun Technical University, TR 31220 Iskenderun, Hatay, Turkey (2) Faculty of Fisheries, Mersin University, Mersin, Turkey Corresponding Author: [email protected]

Abstract: One female specimen of the Squatina oculata was captured by a commercial trawler at a depth of 65 m on 4 November 2017 from Aydıncık coast (North-eastern Mediterranean Sea, Turkey). Squatina oculata had not been reported in this part of the North-eastern Mediterranean Sea nearly for the last two decades. The captured specimen was 726 mm in total length and 3450 g in weight. Morphometric and meristic characters of the captured specimen are compared with the other Mediterranean records. Due to increasing fishing activities and habitat degradation throughout the Mediterranean Sea during the last decades, angelshark species are dramatically declined day by day. Thus, conservation status of the Smoothback Angelshark S. oculata in the Mediterranean Sea is classified as “Critically Endangered” at Global Red List by IUCN.

Résumé : Premier signalement de l’ange de mer ocellé Squatina oculata Bonaparte, 1840 au nord-est de la Méditerranée, Turquie. Un spécimen femelle de l’ange de mer ocellé, Squatina oculata (Bonaparte, 1840), a été capturé (726 mm de longueur totale et 3450 g de poids total) par un chalutier commercial à une profondeur de 65 m le 4 novembre 2017 au large d’Aydıncık (Nord-est de la Méditerranée, Turquie). C’est le premier signalement de S. oculata le long de la côte nord- orientale de la Méditerranée depuis près de deux décennies. Les caractères morphométriques et méristiques du spécimen capturé ont été comparés à d’autres observations en Méditerranée. En raison de l’augmentation des activités de pêche et de la dégradation de l’habitat dans toute la Méditerranée au cours des dernières décennies, les anges de mer déclinent de manière dramatique de jour en jour. Ainsi, l’ange de mer ocellé S. oculata est classé en Méditerranée “en danger critique d’extinction” sur la liste rouge mondiale de l’UICN.

Keywords: Record l Rare species l Squatina oculata l Aydıncık Coast l Turkey

Introduction The genus Squatina Duméril, 1806 is represented by three species in the Mediterranean Sea: , Squatina species are named as and belong to Squatina aculeata Cuvier, 1829 , Angelshark, Squatina the family Squatinidae which has one genus in the world. squatina (Linnaeus, 1758) and Smoothback Angelshark, Squatina oculata Bonaparte, 1840 (Golani et al., 2006; Akyol et al., 2015). The angelsharks are benthic species, Reçu le 15 janvier 2018 ; accepté après révision le 12 juillet 2018. inhabiting tropical and subtropical regions in the eastern Received 15 January 2018; accepted in revised form 12 July 2018. Atlantic coastal waters (Froese & Pauly, 2018). 190 OCCURRENCE OF SQUATINA OCULATA FROM TURKEY

Nowadays, the angelsharks were identified as the second most threatened of all the world’s and rays (Chondrichthyans) after a global review of extinction risk by the International Union for Conservation of Nature (IUCN, 2018) Specialist Group (Dulvy et al., 2014). The Smoothback Angelshark S. oculata was commonly found in warm-temperate and tropical waters of the eastern Atlantic continental shelves and upper slopes from 20 to 500 m, mostly between 50 and 100 m (Compagno, 1984; Serena, 2005). Ondrias (1971) and Roux (1984) stated that it is rarely distributed in the western basin of the Atlantic Ocean. However, Fredj & Maurin (1987) and Fischer et al. (1987) have reported the presence of this species from the western and eastern Mediterranean waters. Nevertheless , this species has been rarely seen in Tunisia (Gulf of Gabes) and more generally in the southern regions of the Mediterranean Sea (Bradai et al., 2006). Figure 1. Map showing the capture sites off Aydıncık, Mersin Although the occurrence of the Smoothback Angelshark Bay (North-Eastern Mediterranean Sea) . species in the Mediterranean has been reported from Turkish coast in previous years (JICA, 1993), this species is extremely rare in the north-eastern part of the specimen was preserved in 4% formalin and was deposited Mediterranean Sea (Golani, 1996; Golani et al., 2006) and in the Museum of Systematic, Faculty of Fisheries, Mersin also throughout the Mediterranean (Kabasakal & University (MEUFC-17-11-037) (Fig. 2). Kabasakal, 2014). After a first confirmed occurrence of S. oculata in the Levantine basin by Golani (1996), this species was reported from Syria (Saad et al., 2006) and Rhodes coast (Corsini & Zava, 2007). S. oculata was recorded for the first time from the eastern Mediterranean coast of Turkey by Başusta & Erdem (2000), and then reported from the Sea of Marmara, the Aegean Sea, and the Levantine Seain the checklist of the marine fishes of Turkey by Bilecenoglu et al. (2002 & 2014). Additionally, Miller (2016) reported an individual of S. oculata from Akyaka in the Aegean Sea coasts of Turkey by local fishermen (Joanna Barker, UK & Europe Project Manager Conservation Programmes, ZSL, personal communication 2015). Very recently, S. oculata was recorded from Italy (Sicily Strait) in the Central Mediterranean Sea (Zava et al., 2016) and the coasts of Syria (Alkusairy & Saad, 2018). The present study contributes to the recent data on the rare occurrences of Smoothback Angelshark S. oculata from Turkish marine waters and reports for the first time the occurrence of a female individual in the North-eastern Figure 2. Squatina oculata. The female specimen from Aydıncık coast, Turkey (Photo: D. Ergüden). Mediterranean Sea, Turkey.

Materials and Methods Results

A single female specimen of S. oculata was caught with a The captured female specimen of S. oculata was 726 mm in commercial trawling on 4 November 2016 at a depth of total length and 3450 g in weight. Morphological features 65 m on sandy bottom from Aydıncık coast (Mersin Bay, of the specimen were provided in table 1 and compared 36°07’350’’N-33°16’250’’E) in the North-eastern with previous observations in the Aegean Sea and Eastern Mediterranean Sea (Fig. 1). Morphometric measurements Mediterranean Sea (Corsini & Zava, 2007; Zava et al., were carried out to the nearest 0.1 mm by a calliper. The D. ERGÜDEN, D. AYAS, M. GÜRLEK, S. KARAN, C. TURAN 191

Table 1. Squatina oculata . Measurements of the individual caught in the North- anterior nasal barbels weakly bifurcated; eastern Mediterranean Sea (Turkey) and compared with previous records posterior margin of anterior nasal flaps caught from the Aegean Sea, Eastern Mediterranean Sea (Corsini & Zava, between nasal barbels and tips weakly fringed; 2007) and the Central Mediterranean Sea (Zava et al., 2016). dermal folds on sides of head without Corsini Present triangular lobes. Origin of first was Measurement (mm) & Zava Zava et al. (2016) study usually well behind free rear tips of pectoral (2007) fins; pectoral fins are low and angular; rear Number n = 1 n = 1 n = 4 tips of pectoral fins were broadly subangular. Sex Female Female Male Male Male Female Large spines were present on snout and above Weight (g) 3.450 3.750 173 625 630 1480 eyes but usually absent from midback; lateral trunk denticles were pointed and with three Total length (TL) 726 795 291 442 432 564 ridges (Compagno, 1984). The color of fresh Standard length (SL) 637 ----- specimen is: body light brown, belly white in Disc length 375 ----- color, prominent white spots on pectoral fins Head length 109 - 52 74 69 87 and on body, three dark black ocelli on both side of caudal peduncle, two large pseudo- Eye diameter 12 15 7 10 11 12 ocelli on pectoral fins, pectoral and pelvic fins Interorbital distance 42 49 --- - margin dusky, dorsal and caudal fins with Pre-orbital length 26 - 10 19 17 20 white margins. Pre- length 53 - 21 35 35 41 The previous and recent records of the Eye-spiracle space 11 12 --- - Angel shark species in Turkish marine waters were summarized in table 2. Distance between spiracles 47 ----- Snout to mouth 33 ----- Discussion Snout to first gill-slit 46 ----- Snout to disc 90 88 --- - The Smoothback Angelshark S. oculata is Snout to first dorsal 435 ----- distinguished from the two other angelshark Snout to pelvic 273 ----- species (i.e. S. aculeata, S. squatina ) by big thorns (sharp, tooth-like structures on the skin) Snout to spiracle 38 ----- that are present on the snout and above the First to second dorsal 51 ----- eyes, a first dorsal fin that originates well Between dorsal bases 28 16 --- - behind the pelvic rear tips, andbrown ocelli Pelvic to caudal space 257 220 95 157 145 200 present in a symmetrical pattern on pectoral fins, tail and on body. S. aculeata differs from Second dorsal to upper 53 ----- the two other angleshark species by having caudal arow of dorsal spines (sword-like bony Pelvic to median tip 73 ----- structure) down the middle of its body, with Upper caudal 76 ----- spines also located on the snout and above the Lower caudal 86 ----- eyes. However, S. squatina can simply be Caudal peduncle height 14 -7810 11 distinguished from these two species by conical nasal barbels, high and wide pectoral Mouth width 54 ----- fins, small spines that are present on snout and Inter gill length 25 - 12 12 16 20 above eyes and may also be present down Inter-nasal width 39 ----- middle of back, and lateral trunk denticles that Inter-spiracular width 47 ----- are very narrow with sharp-cusped crowns (Compagno, 1984; Miller, 2016). Total tooth row in 4 - 3 ----- upper/lower jaws Squatina oculata can reach up to 160 cm in Total teeth in upper/lower 64/54 ----- total length for females with a common length jaws of 120 cm TL while adult males reach a maximal TL of least 145 cm. The size at birth was about 22.6 to 27 cm (Compagno, 1984; 2016). The diagnostic characteristics were similar to those Capapé et al ., 1990 ; Ebert et al., 2013). However, the reported in the previous literature: trunk rather slender; growth rate, reproduction time and longevity of S. oculata 192 OCCURRENCE OF SQUATINA OCULATA FROM TURKEY

Table 2. Records of angelshark species from the Turkish waters in 1983-2017. Record Depth Size TL References Species Location Number Gear Sex date (m) (mm) Gücü & Bingel (1994) S. squatina 1983-1984 North-eastern >1 Bottom 60-78 -- Mediterranean trawl Kabasakal (2003) S. squatina Nov. 1995 Off Kapıdağ, Southern Sea 1 - 50 Female 870 of Marmara Başusta & Erdem (2000) S. oculata 1994-1996 Off Karataş, Southern 1 Bottom 50-60 - 756 Mediterranean Sea trawl Başusta (2002) S. aculeata 15 May Iskenderun Bay, Southern 1 Bottom 120-200 Female 798 1997 Mediterranean Sea trawl Filiz et al. (2005) S. aculeata 01 Apr. Gokova Bay, Aegean Sea 1 Bottom 130 Female 965 2005 trawl Öğretmen et al. (2005) S. squatina 2000-2001 Gökova Bay, South-eastern 1 Trammel --850 Aegean Sea net Karakulak et al. (2006) S. squatina 2004-2005 Gökçeada, Northern Aegean 1 Trammel 30 - 265 Sea net İşmen et al. (2009) S. squatina 2005-2008 Saros Bay, North Aegean 1 Bottom 5-500 Female 232 Sea trawl Kabasakal & Kabasakal S. squatina 04 Jan. Gemlik Bay, Sea of 1 Trammel 50 Female 1740 (2014) 2014 Marmara net Erguden & Bayhan S. aculeata 25 Jun. Mersin Bay, North-eastern 1 Bottom 1-513 Female 690 (2015) 2014 MediterraneanSea trawl Akyol et al. (2015) S. squatina 05 Feb. Gökova Bay, South-eastern 1 Trammel 20 Female 1560 2015 Aegean Sea net S. squatina 07 Feb. Gökova Bay, South-eastern 1 Trammel 47 Female - 2015 Aegean Sea net Başusta (2016) S. aculeata 06 Jun. North-eastern 1 Bottom 415-430 Juvenile 374 2015 Mediterranean Sea trawl This study S. oculata 04 Nov. North-eastern 1 Bottom 65 Female 726 2017 Mediterranean Sea trawl are still not well known. Females are reported to mature at Squatina oculata is classified as “Critically Endangered” 100 cm TL from Tunisian waters and 89 cm from in the Global Red List by the International Union for coastal waters (Capapé et al., 1990 & 2002). Besides, males Conservation of Nature (IUCN, 2018). Gordon et al. (2017) are reported to be mature at 71 cm from Tunisia (Capapé et stated that the Angel Shark Conservation Strategy aims to al., 1990) and 82 cm from Senegal (Capapé et al., 2002). conserve the three Critically Endangered angelshark Recently, Zava et al. (2016) reported four juvenile species ( S. aculeata, S. oculata and S. squatina ) found in specimens (1 female, 3 males) in the Central Mediterranean the Eastern Atlantic and Mediterranean. Thus, they Sea (Strait of Sicily, Italy) with total lengths of 56.4, 44.2, determined key components to improve the overall profile 43.2 and 29.1 cm, respectively. In the present study, the of angelsharks: (i) increase the number of sightings captured female specimen was 72.6 cm TL. Therefore, this reported, (ii) generate a better understanding of current finding of S. oculata described in the present paper is a first distribution to contribute to IUCN Red List re-assessments documented length and weight data of matured female and (iii) identify new opportunities for collaboration. These specimen in the Turkish marine waters. three priority goals will probably play an important role in S. oculata was rarely observed in the eastern the restoration of robust populations and the safeguarding Mediterranean Sea and exploitation data are quite throughout their range of the three species of angelsharks in uncommon. In Syrian coastal waters, the total number of the Eastern Atlantic and Mediterranean Sea. catches of this species in 2002 and in 2006 was given by Ali So far, records of angleshark species (i.e. S. aculeata , S. & Saad (2003) and Saad et al. 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